NF-κB signaling at the crossroads of inflammation and atherogenesis: Searching for new therapeutic links

Expert Opinion on Therapeutic Targets

Volumn 18, Issue 9, 2014, Pages 1089-1101

  Pateras, Ioannis ^a,b   Giaginis, Constantinos ^a,c   Tsigris, Christos ^b   Patsouris, Efstratios ^a   Theocharis, Stamatios ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b UNIVERSITY OF ATHENS   (Greece)

^c UNIVERSITY OF THE AEGEAN   (Greece)

Author keywords

Atherosclerosis pathophysiology; Carotid plague evolution stages; Inflammation; NF B inhibitors enhancers; NF B signaling

Indexed keywords

CELL PROTEIN; CHEMOKINE; HORMONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ANTIINFLAMMATORY AGENT;

ATHEROGENESIS; ATHEROMA; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CAROTID ARTERY; HUMAN; INFLAMMATION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CAROTID ARTERY DISEASES; DRUG DESIGN; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; PLAQUE, ATHEROSCLEROTIC;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ATHEROSCLEROSIS; CAROTID ARTERY DISEASES; DRUG DESIGN; HUMANS; INFLAMMATION; MOLECULAR TARGETED THERAPY; NF-KAPPA B; PLAQUE, ATHEROSCLEROTIC; SIGNAL TRANSDUCTION;

EID: 84906258361     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2014.938051     Document Type: Review

References (100)

1. Brasier AR. The NF-kB regulatory network. Cardiovasc Toxicol. 2006;6(2):111-30
2. Gilmore TD. The Rel/NF-kB signal transduction pathway: introduction. Oncogene 1999;18:6842-4
3. Tian B, Brasier AR. Identification of a nuclear factor k B-dependent gene network. Recent Prog Horm Res 2003;58:95-130
4. Perkins ND. Integrating cell-signalling pathways with NF-kB and IKK function. Nat Rev Mol Cell Biol 2007;8:49-62
5. Gilmore TD. Introduction to NF-kB: players, pathways, perspectives. Oncogene 2006;25:6680-4
6. Mercurio F, Manning AM. Multiple signals converging on NF-kB. Curr Opin Cell Biol 1999;11:226-32
7. Wentzel JJ, Janssen E, Vos J, et al. Extension of increased atherosclerotic wall thickness into high shear stress regions is associated with loss of compensatory remodeling. Circulation 2003;108:17-23
8. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 1999;340:115-26
9. Schoen F, Cotran R. "Blood vessels". In: Cotran RS, Kumar V, Collins T, editors. Robbins pathological basis of disease. W. B. Saunders Company; Philadelphia: 1999
10. Genest JJ Jr, Martin-Munley SS, McNamara JR, et al. Familial lipoprotein disorders in patients with premature coronary artery disease. Circulation 1992;85:2025-33
11. National cholesterol education program report of the national. cholesterol education program expert panel on detection, evaluation, and treatment of high blood cholesterol in adults. Arch Intern Med 1988;148:36
12. Baldwin AS. The NF-kB and IkB proteins: new discoveries and insights. Annu Rev Immunol 1996;14:649-83
13. Ghosh S, May MJ, Kopp EB. NF-kB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998;16:225-60
14. Basak S, Kim H, Kearns JD, et al. A fourth IkB protein within the NF-kB signaling module. Cell 2007;128:369-81
15. Henkel T, Zabel U, van Zee K, et al. Intramolecular masking of the nuclear location signal and dimerization domain in the precursor for the p50 NF-kB subunit. Cell 1992;68:1121-33
16. Abraham E. NF-kB activation. Crit Care Med 2000;28(4):100-4
17. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation 2002;105:1135-43
18. Yaron A, Gonen H, Alkalay I, et al. Inhibition of NF-kB cellular function via specific targeting of the I-kB-ubiquitin ligase. EMBO J 1997;16:6486-94
19. Shishehbor MH, Bhatt DL. Inflammation and atherosclerosis. Curr Atheroscler Rep 2004;6:131-9
20. Vanepps JS, Vorp DA. Mechanopathobiology of atherogenesis: a review. J Surg Res 2007;142:202-17
21. Libby P. Molecular bases of the acute coronary syndromes. Circulation 1995;91:2844-50
22. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 2003;362:801-9
23. Messner B, Bernhard D. Smoking and cardiovascular disease: mechanisms of endothelial dysfunction and early atherogenesis. Arterioscler Thromb Vasc Biol 2014;34:509-15
24. Gimbrone MA Jr. Culture of vascular endothelium. Prog Hemostat Thromb 1976;3:1-28
25. Stoneman VE, Bennett MR. Role of apoptosis in atherosclerosis and its therapeutic implications. Clin Sci (Lond) 2004;107:343-54
26. Penn MS, Rangaswamy S, Saidel GM, et al. Macromolecular transport in the arterial intima: comparison of chronic and acute injuries. Am J Physiol 1997;272:H1560-70
27. Mehta JL, Chen J, Hermonat PL, et al. Lectin-like, oxidized low-density lipoprotein receptor-1 (LOX-1): a critical player in the development of atherosclerosis and related disorders. Cardiovasc Res 2006;69:36-45
28. Leake DS, Rankin SM. The oxidative modification of lowdensity lipoproteins by macrophages. Biochem J 1990;270:741-8
29. Steinberg D. Lipoprotein modification and atherogenesis. Arterioscler Rev 1991;23:115-21
30. Faggiotto A, Ross R, Harker L. Studies of hypercholesterolemia in the nonhuman primate. I. Changes that lead to fatty streak formation. Arteriosclerosis 1984;4:323-40
31. Goldstein JL, Ho YK, Basu SK. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci USA 1979;76:333-7
32. Ross R. The pathogenesis of atherosclerosis - an update. N Engl J Med 1986;314:488-500
33. Gown AM, Tsukada T, Ross R. Human atherosclerosis. II. Immunocytochemical analysis of the cellular composition of human atherosclerotic lesions. Am J Pathol 1986;125:191-207
34. Jonasson L, Holm J, Skalli O, et al. Regional accumulations of T cells, macrophages, and smooth muscle cells in the human atherosclerotic plaque. Arteriosclerosis 1986;6:131-8
35. Davies MJ, Woolf N, Rowles PM, et al. Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. Br Heart J 1988;60:459-64
36. Reape TJ, Groot PH. Chemokines and atherosclerosis. Atherosclerosis 1999;147(2):213-25
37. Huo Y, Ley K. Adhesion molecules and atherogenesis. Acta Physiol Scand 2001;173:35-43
38. Hulthe J, Fagerberg B. Circulating oxidized LDL is associated with subclinical atherosclerosis development and inflammatory cytokines (AIR Study). Arterioscler Thromb Vasc Biol 2002;22:1162-7
39. Huber J, Boechzelt H, Karten B, et al. Oxidized cholesteryl linoleates stimulate endothelial cells to bind monocytes via the extracellular signal-regulated kinase 1/2 pathway. Arterioscler Thromb Vasc Biol 2002;22:581-6
40. Boring L, Gosling J, Cleary M, et al. Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 1998;394:894-7
41. Yamada Y, Doi T, Hamakubo T, et al. Scavenger receptor family proteins: roles for atherosclerosis, host defence and disorders of the central nervous system. Cell Mol Life Sci 1998;54:628-40
42. Kansas GS. Selectins and their ligands: current concepts and controversies. Blood 1996;88:3259-87
43. Johnson-Tidey RR, McGregor JL, Taylor PR, et al. Increase in the adhesion molecule P-selectin in endothelium overlying atherosclerotic plaques. Coexpression with intercellular adhesion molecule-1. Am J Pathol 1994;144:952-61
44. Manka DR, Wiegman P, Din S, et al. Arterial injury increases expression of inflammatory adhesion molecules in the carotid arteries of apolipoprotein-Edeficient mice. J Vasc Res 1999;36:372-8
45. Libby P. Inflammation in atherosclerosis. Nature 2002;420:868-74
46. Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 2011;17:1410-22
47. Faggiotto A, Ross R, Harker L. Studies of hypercholesterolemia in the nonhuman primate. I. Changes that lead to fatty streak formation. Arteriosclerosis 1984;4:323-40
48. de Boer OJ, van der Wal AC, Teeling P, et al. Leucocyte recruitment in rupture prone regions of lipid-rich plaques: a prominent role for neovascularization? Cardiovasc Res 1999;41:443-9
49. Brogi E, Winkles JA, Underwood R, et al. Distinct patterns of expression of fibroblast growth factors and their receptors in human atheroma and non-atherosclerotic arteries: association of acidic FGF with plaque microvessels and macrophages. J Clin Invest 1993;92:2408-18
50. Ramos MA, Kuzuya M, Esaki T, et al. Induction of macrophage VEGF in response to oxidized LDL and VEGF accumulation in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol 1998;18:1188-96
51. Jeziorska M, Woolley DE. Local neovascularization and cellular composition within vulnerable regions of atherosclerotic plaques of human carotid arteries. J Pathol 1999;188:189-96
52. Martín-Ventura JL, Madrigal-Matute J, Muñoz-Garcia B, et al. Increased CD74 expression in human atherosclerotic plaques: contribution to inflammatory responses in vascular cells. Cardiovasc Res 2009;83:586-94
53. Henne C, Schwenk F, Koch N, et al. Surface expression of the invariant chain (CD74) is independent of concomitant expression of major histocompatibility complex class II antigens. Immunology 1995;84:177-82
54. Starlets D, Gore Y, Binsky I, et al. Cellsurface CD74 initiates a signaling cascade leading to cell proliferation and survival. Blood 2006;107:4807-16
55. Basta G. Receptor for advanced glycation endproducts and atherosclerosis: from basic mechanisms to clinical implications. Atherosclerosis 2008;196:9-21
56. Price CL, Knight SC. Advanced glycation: a novel outlook on atherosclerosis. Curr Pharm Des 2007;13:3681-7
57. Montecucco F, Steffens S, Mach F. Insulin resistance: a proinflammatory state mediated by lipid-induced signaling dysfunction and involved inatherosclerotic plaque instability. Mediators Inflamm 2008;2008:767623
58. Rask-Madsen C, King GL. Proatherosclerotic mechanisms involving protein kinase C in diabetes and insulin resistance. Arterioscler Thromb Vasc Biol 2005;25:487-96
59. Mas S, Martínez-Pinna R, Martín-Ventura JL, et al. Local non-esterified fatty acids correlate with inflammation in atheroma plaques of patients with type 2 diabetes. Diabetes 2010;59:1292-301
60. Lopez-Franco O, Hernandez-Vargas P, Ortiz-Munoz G, et al. Parthenolide modulates the NF-kappaB-mediated inflammatory responses in experimental atherosclerosis. Arterioscler Thromb Vasc Biol 2006;26:1864-70
61. Tedgui A, Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 2006;86:515-81
62. Barlic J, Murphy PM. Chemokine regulation of atherosclerosis. J Leukoc Biol 2007;82:226-36
63. Zernecke A, Weber C. Chemokines in the vascular inflammatory response of atherosclerosis. Cardiovasc Res 2010;86:192-201
64. Calvayrac O, Rodríguez-Calvo R, Alonso J, et al. CCL20 is increased in hypercholesterolemic subjects and is upregulated by LDL in vascular smooth muscle cells: role of NF-kB. Arterioscler Thromb Vasc Biol 2011;31:2733-41
65. Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev 2003;14:409-26
66. Ghadjar P, Rubie C, Aebersold DM, et al. The chemokine CCL20 and its receptor CCR6 in human malignancy with focus on colorectal cancer. Int J Cancer 2009;125:741-5
67. Liao YC, Wang YS, Guo YC, et al. BRAP activates inflammatory cascades and increases the risk for carotid atherosclerosis. Mol Med 2011;17:1065-74
68. Ozaki K, Sato H, Inoue K, et al. SNPs in BRAP associated with risk of myocardial infarction in Asian populations. Nat Genet 2009;41:329-33
69. de Winther MP, Kanters E, Kraal G, et al. Nuclear factor kappaB signaling in atherogenesis. Arterioscler Thromb Vasc Biol 2005;25(5):904-14
70. Tilstam PV, Gijbels MJ, Habbeddine M, et al. Bone marrow-specific knock-in of a non-activatable Ikka kinase mutant influences haematopoiesis but not atherosclerosis in Apoe-deficient mice. PLoS One 2014;9:e87452
71. Dhar K, Rakesh K, Pankajakshan D, et al. SOCS3 promotor hypermethylation and STAT3-NF-kB interaction downregulate SOCS3 expression in human coronary artery smooth muscle cells. Am J Physiol Heart Circ Physiol 2013;304:H776-85
72. Sattler KJ, Woodrum JE, Galili O, et al. Concurrent treatment with renninangiotensin system blockers and acetylsalicylic acid reduces nuclear factor kappaB activation and C-reactive protein expression in human carotid artery plaques. Stroke 2005;36:14-20
73. Coletta AP, Cleland JGF, Freemantle N, et al. Clinical trials update from the European Society of Cardiology: CHARM, BASEL, EUROPA, and ESTEEM. Eur J Heart Fail 2003;5:697-704
74. Bosch J, Yusuf S, Pogue J, et al. Use of ramipril in preventing stroke: double blind randomised trial. BMJ 2002;324:699-702
75. Eidelman RS, Hebert PR, Weisman SM, et al. An update on aspirin in the primary prevention of cardiovascular disease. Arch Intern Med 2003;163:2006-10
76. Martín-Ventura JL, Blanco-Colio LM, Gómez-Hernández A, et al. Intensive treatment with atorvastatin reduces inflammation in mononuclear cells and human atherosclerotic lesions in one month. Stroke 2005;36:1796-800
77. Nissen SE, Tuzcu EM, Schoenhagen P, et al. Effect of intensive compared with moderate lipid-lowering therapy on progression of coronary atherosclerosis: a randomized controlled trial. J Am Med Assoc 2004;291:1071-80
78. Wehinger A, Tancevski I, Seiler R, et al. Influence of aspirin on SR-BI expression in human carotid plaques. Atherosclerosis 2009;206:234-8
79. Acton S, Rigotti A, Landschulz KT, et al. Identification of scavenger receptor SRBI as a high density lipoprotein receptor. Science 1996;271:518-20
80. Cronstein BN, Weissmann G. Targets for antiinflammatory drugs. Annu Rev Pharmacol Toxicol 1995;35:449-62
81. Awtry EH, Loscalzo J. Aspirin. Circulation 2000;101:1206-18
82. Neri Serneri GG, Coppo M, Bandinelli M, et al. Exaggerated myocardial oxLDL amount and LOX-1 receptor overexpression associated with coronary microvessel inflammation in unstable angina. Atherosclerosis 2013;226:476-82
83. Martín-Ventura JL, Blanco-Colio LM, Muñoz-García B, et al. NF-kappaB activation and Fas ligand overexpression in blood and plaques of patients with carotid atherosclerosis: potential implication in plaque instability. Stroke 2004;35:458-63
84. Nagata S. Fas ligand-induced apoptosis. Annu Rev Genet 1999;33:29-55
85. Geng YJ, Henderson LE, Levesque EB, et al. Fas is expressed in human atherosclerotic intima and promotes apoptosis of cytokine-primed human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1998;17:2200-8
86. Park L, Raman KG, Lee KJ, et al. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med 1998;4:1025-31
87. Bucciarelli LG, Wendt T, Qu W, et al. RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein-E-null mice. Circulation 2002;106:2827-35
88. Hudson BI, Harja E, Moser B, et al. Soluble levels of receptor for advanced glycation endproducts (sRAGE) and coronary artery disease: the next Creactive protein? Arterioscler Thromb Vasc Biol 2005;25:879-82
89. Cuccurullo C, Iezzi A, Fazia ML, et al. Suppression of RAGE as a basis of simvastatin-dependent plaque stabilization in type 2 diabetes. Arterioscler Thromb Vasc Biol 2006;26:2716-23
90. Marfella R, Di Filippo C, Portoghese M, et al. Proteasome activity as a target of hormone replacement therapy-dependent plaque stabilization in postmenopausal women. Hypertension 2008;51:1135-41
91. Marfella R, Ferraraccio F, Rizzo MR, et al. Innate immune activity in plaque of patients with untreated and L-thyroxinetreated subclinical hypothyroidism. J Clin Endocrinol Metab 2011;96:1015-20
92. Herrmann J, Ciechanover A, Lerman LO, et al. The ubiquitin proteasome system in cardiovascular diseases-a hypothesis extended. Cardiovasc Res 2004;61:11-21
93. Taddei S, Caraccio N, Virdis A, et al. Impaired endothelium dependent vasodilatation in subclinical hypothyroidism: beneficial effect of levothyroxine therapy. J Clin Endocrinol Metab 2003;88:3731-7
94. Kvetny J, Heldgaard PE, Bladbjerg EM, et al. Subclinical hypothyroidism is associated with a low-grade inflammation, increased triglyceride levels and predicts cardiovascular disease in males below 50 years. Clin Endocrinol (Oxf) 2004;61:232-8
95. Sigala F, Savvari P, Liontos M, et al. Increased expression of bFGF is associated with carotid atherosclerotic plaques instability engaging the NF-kappaB pathway. J Cell Mol Med 2010;14:2273-80
96. Grochot-Przeczek A, Dulak J, Jozkowicz A. Therapeutic angiogenesis for revascularization in peripheral artery disease. Gene 2013;525:220-8
97. Bernal-Lopez MR, Garrido-Sanchez L, Gomez-Carrillo V, et al. Antioxidized LDL antibodies are associated with different metabolic pathways in patients with atherosclerotic plaque and type 2 diabetes. Diabetes Care 2013;36:1006-11
98. Gareus R, Kotsaki E, Xanthoulea S, et al. Endothelial cell-specific NF-kappaB inhibition protects mice from atherosclerosis. Cell Metab 2008;8:372-83
99. Collins T, Cybulsky MI. NF-kB: pivotal mediator or innocent bystander in atherogenesis? J Clin Invest 2001;107:255-64
100. Monaco C, Andreakos E, Kiriakidis S, et al. Canonical pathway of nuclear factor kappa B activation selectively regulates proinflammatory and prothrombotic responses in human atherosclerosis. Proc Natl Acad Sci USA 2004;101:5634-9